Abstract
Climate is altering rapidly in parts of the Arctic and Antarctic but we know little about how marine organisms are responding to, or might respond to such changes. Knowledge of within-taxon variability is the vital context (currently missing) to interpretation of environmental signals. We investigated growth in six species and three genera of erect Antarctic bryozoans, an ideal model taxon to investigate such response. Cellarinella margueritae, C. nodulata, C. rogickae, C. watersi, Melicerita obliqua and Stomhypselosaria watersi, extended 3.4, 5.2, 4.6, 4.1, 4.9 and 4.5 mm year−1 and synthesised 24, 55, 45, 176, 34 and 46 mg CaCO3 year−1, respectively. The maximum ages of these species ranged from 11 to 15 years except M. obliqua, which reached 32 years. This is the first investigation of growth rates of closely related Antarctic invertebrate species and reports the slowest growth rates of bryozoans known from anywhere to date. Our data coupled with that from literature shows that Antarctic bryozoan growth varies <<101 between species, 101 between genera, 102 between morphologies and is ∼101 slower than in tropical or temperate regions. However, within encrusting types the slowest growing species grow at similar rates from poles to tropics. Age was a strong confounding factor across our Antarctic study species but age-standardised data showed a possible decline in annual growth from 1992 to 2003. We identify several factors increasing this environmental signal strength, including (1) the importance of generic (though not necessarily species) identification and (2) use of dry-mass or ash-free dry-mass as the measures of growth.
Similar content being viewed by others
References
Arntz WE, Brey T, Gallardo VA (1994) Antarctic zoobenthos. Oceanogr Mar Biol Ann Rev 32:241–304
Bader B (2000) Life cycle, growth rate, and carbonate production of Cellaria sinuosa. In: Herrera Cubilla A, Jackson JBC (eds) Proceedings of the 11th international bryozoology association conference. Smithsonian Tropical Research Institute, Balboa, pp 136–144
Bader B, Schäfer P (2004) Skeletal morphogenesis and growth check lines in the Antarctic bryozoan Melicerita obliqua. J Nat Hist 38:2901–2922
Barnes DKA (1995) Seasonal and annual growth in erect species of Antarctic bryozoans. J Exp Mar Biol Ecol 188:181–198
Barnes DKA, Arnold RJ (2001) A growth cline in encrusting benthos along a latitudinal gradient within Antarctic waters. Mar Ecol Prog Ser 210:85–91
Barnes DKA, Clarke A (1994) Seasonal variation in the feeding activity of four species of Antarctic bryozoan in relation to environmental factors. J Exp Mar Biol Ecol 181:117–133
Barnes DKA, Kuklinski P (2005) Low colonisation on artificial substrata in arctic Spitsbergen. Polar Biol. doi:10.1007/s00300-005-0044-y
Barnes DKA, Peck LS (2005) Extremes of metabolic strategy in Antarctic Bryozoa. Mar Biol 147:979–988
Barnes DKA, Webb K, Linse K (2006) Slow growth of Antarctic bryozoans increases over 20 years and is anomalously high in 2003. Mar Ecol-Prog Ser 314:187–195
Bowden DA, Clarke A, Peck LS, Barnes DKA (2006) Antarctic sessile marine benthos: colonization and growth on artificial substrata over 3 yr. Mar Ecol-Prog Ser 316:1–16
Brey T, Mackensen A (1997) Stable isotopes prove shell growth bands in the Antarctic bivalve Laternula elliptica to be formed annually. Polar Biol 17:465–468
Brey T, Peck LS, Gutt J, Hain S, Arntz W (1995) Population dynamics of Magellania fragilis, a brachiopod dominating a mixed-bottom macrobenthic assemblage on the Antarctic shelf. J Mar Biol Ass UK 75:857–870
Brey T, Gutt J, Mackensen A, Starmans A (1998) Growth and productivity of the high Antarctic bryozoan Melicerita obliqua. Mar Biol 132:327–333
Brey T, Gerdes D, Gutt J, Mackensen A, Starmans A (1999) Growth and age of the Antarctic bryozoan Cellaria incula on the Weddell Sea shelf. Antarct Sci 11:408–414
Buick DP, Ivany LC (2004) 100 years in the dark: Extreme longevity of Eocene bivalves from Antarctica. Geology 32:921–924
Clarke A (1988) Seasonality in the Antarctic marine environment. Comp Biochem Physiol 90B:461–473
Clarke A, North AW (1991) Is the growth of polar fish limited by temperature? In: di Prisco G, Maresca B, Tota B (eds) Biology of Antarctic fish. Springer, Heidelberg, pp 54–69
Clarke A, Prothero-Thomas E, Beaumont J, Chapman AL, Brey T (2005) Growth in the limpet Nacella concinna from contrasting sites in Antarctica. Polar Biol 28:62–71
Cocito S, Novosel M, Pasaric Z, Key MM (2006) Growth of the bryozoan Pentapora fascialis (Cheilostomata, Ascophora) around submarine freshwater springs in the Adriatic Sea. Linzer biol Beitr 38:15–24
Comiso JC (2000) Variability and trends in Antarctic surface temperatures from in situ and satellite infrared measurements. J Geophys Res 91:975–994
Dayton PK (1979) Observations of growth, dispersal and dynamics of some sponges in McMurdo sound, Antarctica, and its biological effects. In: Levian C, Bourny-Esnault (eds) Sponge biology. Centre National de la Recherche Scientifique, Paris, pp 271–283
Dayton PK (1989) Interdecadal variation in an Antarctic sponge and its predators from oceanographic climate shifts. Science 245:1484–1486
Dayton PK (1990) Polar benthos. In: Smith WO (ed) Polar oceanography. Academic, London, pp 631–685
Gruzov EN (1977) Seasonal alterations in coastal communities in the Davis Sea. In: Llano GA (ed) Adaptations within Antarctic ecosystems. Smithsonian Institution, Balboa, pp 263–278
Hayward PJ (1995) Antarctic cheilostomatous bryozoa. Oxford University Press, Oxford, p 355
Hermansen P, Larsen PS, Riisgard HU (2001) Colony growth rate of encrusting marine bryozoans (Electra pilosa and Celleporella hyalina). J Exp Mar Biol Ecol 263:1–23
Herrera A, Jackson JBC (1996) Life history variation among ‘dominant’ encrusting cheilostomate Bryozoa. In: Gordon DP, Smith AM, Grant-Mackie JA (eds) Bryozoans in space and time. NIWA, Wellington, pp 117–123
Hillmer G, Scholz J, Dullo W-C (1996) Two types of bryozoan nodules from the Gulf of Aqaba, Red Sea. In: Gordon DP, Smith AM, Grant-Mackie J (eds) Bryozoans in space and time. NIWA, Wellington, pp 125–130
King JC, Harangozo SA (1998) Climate change in the western Antarctic Peninsula since 1945:observations and possible causes. Ann Glaciol 27:571–575
Kowalke J, Tatian M, Sahade R, Arntz WE (2001) Production and respiration of Antarctic ascidians. Polar Biol 24:663–669
Lutz RA, Rhodes DC (1980) Growth patterns within the molluscan shell: an overview. In: Rhodes DC, Lutz RA (eds) Skeletal growth of aquatic organisms. Plenum Press, New York, pp 203–254
McKinney ML, Lockwood J (1999) Biotic homogenisation: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453
Meredith MP, King JC (2005) Climate change in the ocean to the west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Let 32:L19604. doi:10.1029/2005GL024042, 2005
O’Dea A, Jackson JBC (2002) Bryozoan growth mirrors contrasting seasonal regimes across the Isthmus of Panama. Palaeogeogr Palaeoclimatol Palaeoecol 185:77–94
O’Dea A, Okamura B (1999) Influence of seasonal variation in temperature, salinity and food availability on module size and colony growth of the estuarine bryozoan Conopeum seurati. Mar Biol 135:581–588
Pätzold J, Ristedt H, Wefer G (1987) Rate of growth and longevity of a large colony of Pentapora foliacea (Bryozoa) recorded in their oxygen isotope profiles. Mar Biol 96:535–538
Pearse JS, McClintock JB, Bosch I (1991) Reproduction in Antarctic benthic marine invertebrates: tempos, modes and timing. Am Zool 31:65–80
Peck LS (2002) Ecophysiology of Antarctic marine ectotherms: limits to life. Polar Biol 25:31–40
Peck LS, Brey T (1996) Bomb signals in old antarctic brachiopods. Nature 380:207–208
Poulin E, Palma AT, Féral J-P (2002) Evolutionary versus ecological success in Antarctic benthic invertebrates. Trends Ecol Evol 17:218–222
Quayle WC, Peck LS, Ellis-Evans CJ, Peat HJ, Harrigan PR (2002) Extreme responses to climate change in Antarctic lakes. Science 295:645
Rauschert M (1991) Ergebnisse der faunistischen arbeiten im benthal von King George Island (Südshetlandinseln, Antarktis). Ber Polarforsch 76:1–75
Schäfer P (1994) Growth strategies of Arctic bryozoa in the Nordic Seas. In: Hayward PJ, Ryland JS, Taylor PD (eds) Biology and palaeobiology of bryozoans, Olsen & Olsen, Fredensborg, pp 173–176
Smith AM, Key MM (2004) Controls, variation, and a record of climate change in detailed stable isotope record in a single bryozoan skeleton. Quat Res 61:123–133
Smith AM, Nelson CS (1994) Calcification rates of rapidly colonizing bryozoans in Haukuri Gulf, northern New Zealand. N Z J Mar Freshw Res 28:227–234
Smith AM, Stewart B, Key MM, Jamet CM (2001) Growth and carbonate production by Adeonellopsis (Bryozoa: Cheilostomata) in Doubtful Sound, New Zealand. Palaeogeog Palaeoclimat Palaeoecol 175:201–210
Stebbing ARD (1971) Growth of Flustra foliacea (Bryozoa). Mar Biol 9:267–273
Stanwell-Smith D, Barnes DKA (1997) Benthic community development in Antarctica: recruitment and growth on settlement panels at Signy Island. J Exp Mar Biol Ecol 212:61–79
Tanaka K (2002) Growth dynamics and mortality of the intertidal encrusting sponge Halichondria okadai (Demospongiae, Halichondrida). Mar Biol 140:383–390
Taylor PD, Voigt E (1999) An unusually large cyclostome (Pennipora anomalopora) from the Upper Cretaceous of Maastricht. Bull Inst R Sci Nat Belg Sci Terre 69:165–171
Taylor PD, Wilson MA (2003) Palaeoecology and evolution of marine hard substrate communities. Earth-Sci Rev 62:1–103
Teixido N, Garrabou J, Gutt J, Arntz WE (2004) Recovery in Antarctic benthos after iceberg disturbance: trends in benthic composition, abundance and growth forms. Mar Ecol Prog Ser 278:1–16
Vail LL, Wass RE (1981) Experimental studies on the settlement and growth of bryozoa in the natural environment. Aus J Mar Freshwat Res 32:639–656
Voigt M (2004) Wachstumsschwankungen der antarktischen Muschel Laternula elliptica in den letzten vierzig Jahren im Gebiet von King George Island. Unpublished PhD thesis, Universität Rostock, Germany
Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological response to recent climate change. Nature 416:389–395
Wasson K, Newberry AT (1997) Modular animals: gonochoric, hermaphroditic, or both at once? Invert Reprod Dev 31:159–175
Winston JE (1983) Patterns of growth, reproduction and mortality in bryozoans from the Ross Sea, Antarctica. Bull Mar Sci 33:688–702
Winston JE, Jackson JBC (1984) Ecology of cryptic coral reef communities 4. Community development and life histories of encrusting cheilostome Bryozoa. J Exp Mar Biol Ecol 76:1–21
Acknowledgments
We thank W.E. Arntz (Alfred Wegner Institute, Germany) to enable K. Linse’s participation in ANT XXI-2 and the helpful colleagues and ship’s crew on PFS Polarstern. We thank Peter Fretwell for preparation of Fig. 1 and Prof Andrew Clarke and three anonymous referees for comments leading to an improved manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Barnes, D.K.A., Webb, K.E. & Linse, K. Growth rate and its variability in erect Antarctic bryozoans. Polar Biol 30, 1069–1081 (2007). https://doi.org/10.1007/s00300-007-0266-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-007-0266-2